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The Antiviral Effect of Indonesian Medicinal Plant Extracts Against pathogens Article The Antiviral Effect of Indonesian Medicinal Plant Extracts Against Dengue Virus In Vitro and In Silico Rosmalena Rosmalena 1, Berna Elya 2, Beti E. Dewi 3, Fithriyah Fithriyah 3, Hidayati Desti 3, Marissa Angelina 4, Muhammad Hanafi 4, Puspa D. Lotulung 4, Vivitri D. Prasasty 5 and Dimas Seto 3,* 1 Department of Medical Chemistry, Faculty of Medicine, Universitas Indonesia, Depok, Jawa Barat 16424, Indonesia; [email protected] 2 Faculty of Pharmacy, Universitas Indonesia, Depok, Jawa Barat 16424, Indonesia; [email protected] 3 Department of Microbiology, Faculty of Medicine, Universitas Indonesia-Cipto Mangukusumo Hospital, Jalan Pengangsaan Timur No. 16, Jakarta 10320, Indonesia; [email protected] (B.E.D.); [email protected] (F.F.); [email protected] (H.D.) 4 Research Centre for Chemistry LIPI, Kompleks Puspiptek, Serpong 15416, Indonesia; [email protected] (M.A.); hanafi[email protected] (M.H.); [email protected] (P.D.L.) 5 Faculty of Biotechnology, Atma Jaya Catholic University of Indonesia, Jalan Jenderal Sudirman 51, Jakarta 12930, Indonesia; [email protected] * Correspondence: [email protected] Received: 7 May 2019; Accepted: 19 June 2019; Published: 22 June 2019 Abstract: Dengue infections are still a worldwide burden, especially in Indonesia. There is no specific medication against the dengue virus. Recently, many types of research have been conducted to discover a new drug for dengue virus using natural resource extracts. Indonesia, as a tropical country, has a wide biodiversity. There are several medicinal plants in Indonesia that are believed to possess anti-dengue activity, such as Myristica fatua, Cymbopogon citratus, and Acorus calamus plants. We conducted an in vitro laboratory experiment of several extracts from Indonesian herbs combined with in silico analysis. The extracts were evaluated for safety and antiviral activity in Huh7it-1 cell lines, using a single dose of 20 µg/mL and dose-dependent (5, 10, 20, 40, 80 and 160 µg/mL) of plant extracts against dengue virus serotype 2 (DENV-2) NGC strain. The DMSO 0.1% was used as a negative control. The cytotoxic aspect was assessed by counting the cell viability, while the antiviral activity was calculated by counting the average inhibition. The selectivity index (SI) of plant extracts were performed from a ratio of CC50/EC50 value. In silico analysis was conducted to determine the free energy of binding between NS5 of dengue virus with bioactive compounds contained in Myristica fatua, Cymbopogon citratus and Acorus calamus extract plants. We determined that all extracts were not toxic against Huh7it-1 cell lines. The methanolic extracts of A. calamus, C. citratus, and M. fatua showed inhibition of DENV-2 at a dose of 20 µg/mL to 96.5%, 98.9%, and 122.7%, respectively. The dose-dependent effects showed that M. fatua has the best inhibition activity towards DENV-2. Molecular docking result showed that artesunic acid within M. fatua has the best free energy of binding ( 7.2 kcal/mol), followed by homoegonol ( 7.1 kcal/mol) which was slightly different from − − artesunic acid among others. The methanolic extracts of A. calamus, C. citratus, and M. fatua showed prospective anti-dengue activities both in vitro and in silico. Future research should be conducted to find the pure extracts of all useful herbs as a new candidate of antiviral drug. Keywords: Plant extract; dengue virus; antiviral activity; Acorus calamus; Cymbopogon citratus; Myristica fatua Pathogens 2019, 8, 85; doi:10.3390/pathogens8020085 www.mdpi.com/journal/pathogens Pathogens 2019, 8, 85 2 of 11 1. Introduction It has estimated that 390 million dengue infections occur worldwide annually [1]. Several outbreaks occurred almost in every place in the world, especially in the Asia region [2]. In Indonesia, there was approximately 800,000 total dengue cases and 200,000 hospitalized cases in 2015 [3]. Dengue virus consists of 4 serotypes, namely dengue virus serotype 1 (DENV-1), serotype 2 (DENV-2), serotype 3 (DENV-3), and serotype 4 (DENV-4), with all of them circulating in Indonesia [4,5]. Besides Indonesia, the other Asian countries where outbreaks of DENV have been substantial were Malaysia, the Philippines, Thailand, and Vietnam; while some Latin America locations including Brazil, Colombia, Honduras, Mexico, and Puerto Rico, were affected during 2011–2014. The burdens varied widely according to country, however, the rates were generally higher and the disease was more frequently severe in Asian countries than in Latin American countries [6]. Currently, there is no specific treatment for dengue infection. However, appropriate medical treatment could save the lives of patients [7]. Clinical manifestations of DENV infection range from asymptomatic: Dengue Fever (DF), Dengue Hemorrhagic Fever (DHF), ultimately Dengue Shock Syndrome (DSS) [8]. The preventive measures for mitigating dengue infection are mainly vector control and proposed dengue vaccine [6]. Research in dengue vaccine has shown some promise in preventing severe dengue cases but still has a long way to go [7]. One of the most critical issues of new antiviral drug development is the in vitro model experiment to be used. The cell substrate requirements for virus replication limit the screening of new compounds. For this reason, only a few drugs have arisen as efficient antiviral agents [9]. As an alternative, several medicinal plant extracts had been investigated to develop a new antiviral drug for dengue [8]. Some of the phytochemical compounds such as flavonoid, phenolics, and terpenoid that could be extracted from natural products were suggested to have an antiviral feature against dengue [10]. Indonesian plants such as Curcuma longa had been investigated as a potential antiviral against DENV and showed promising results [11]. The main objective of this study was to evaluate the effectiveness of plant extracts from Myristica fatua, Acorus calamus, and Cymbopogon citratus as antiviral agents against dengue virus infection in human Huh7it-1 cell lines in vitro and molecular docking in silico. The specific objectives were: i) to optimize the antiviral assay for dengue virus, ii) to measure the CC50 and EC50 of plant extracts in vitro, iii) to determine the selectivity index (SI) of plant extracts towards DENV, and iv) to predict the free energy of binding of antiviral agents with DENV protein target. 2. Results The antiviral assay is essential to examine the maximum non-toxic concentration (MNTC) of the extract that is not toxic to the cells in the first step. After the MNTC of the extracts was assessed, 20 µg/mL of A. calamus, C. citratus and M. fatua, then were applied to Huh7it-1 cells infected by DENV. The result of Huh7it-1 cell lines treated with 20 µg/mL of three crude extracts showed different cytotoxic effects. Table1 revealed that all of the extracts tested in this study were considered as being safe treatments with a range of cell viability in vitro assays that varied from 96.5% to 122.7%. Thus, it suggested that there was no significant cytotoxic effect on the Huh7 it-1 cell lines. Table 1. Viability of selected plant extracts on Huh7it-1 cells at a single dose of 20 µg/mL. Methanolic Extract Cell Viability (%) Acorus calamus 96.5 Cymbopogon citratus 98.9 Myristica fatua 122.7 The percentage of infectivity reduction of plant extracts and inhibition of DENV-2 NGC strain in Huh7it-1 cell was shown in Table2. This result showed that the methanolic extract of Myristica fatua Pathogens 2019, 8, 85 3 of 11 and Cymbopogon citratus gave over than 50% inhibition of DENV-2 NGC strain in vitro. Moreover, methanolic extract of three plant extracts with 20 µg/mL may vary in DENV infectivity and inhibition effects, with high viability of the cells (Tables1 and2). Further research needs to be conducted to isolate and characterize the pure compounds from three those plant extracts with antiviral activities. Table 2. Percentage of infectivity and inhibition of DENV-2 on Huh7it-1 cell lines. Sample Average Infectivity (%) Average Inhibition (%) Acorus calamus (leaves methanol extract) 73.4 26.6 Cymbopogon citratus (root methanol extract) 47.8 52.2 Myristica fatua (methanol extract) 21.6 78.4 To deepen investigation towards plant extract on antiviral aspects, DENV were treated with various concentration of extract before infected to the Huh7it-1 cells. The plant extract concentrations were used: 160 µg/mL, 80 µg/mL, 40 µg/mL, 20 µg/mL, 10 µg/mL, and 5 µg/mL, respectively. DMSO 0.1% was used as a negative control. To obtain assurance that plant extracts were not toxic to the cell, the half cytotoxic concentrations (CC50) were determined. This was achieved from the result of the MTT assay. The cell viability still showed a high level after being treated with plant extracts at concentrations of up to 40 µg/mL for A. calamus and M. fatua extracts, while C. citratus extract showed decreased cell viability after 20 µg/mL. The other in vitro parameter has been defined in an attempt to quantify the effectiveness of antiretroviral agents, most importantly the 50% effective concentrations (EC50) as inhibition of viral replication or symptoms in an appropriate cell culture treatment of the disease. The viral replication inhibition increased as the three plant extract concentrations increased. This indicated that there were antiviral activities from those three plant extracts to DENV. From the ratio equation between CC50 and EC50, the SI of three plant extracts are shown on Table3. Table 3. The 50% cytotoxic (CC50) and 50% inhibition (IC50) concentrations, and selective index (SI) of plant extracts against DENV on Huh7it-1 cell lines. 1 1 Plant Extract CC50 (µg.mL− ) EC50 (µg.mL− ) SI Acorus calamus 424.93 n.d.* n.d. Cymbopogon citratus 183.74 29.37 6.26 Myristica fatua 474.42 25.33 18.73 n.d.
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